By the mid-1980s, the federal government was looking for a way out of the airport business. The FAA had operated Washington National since the airport opened in 1941 and Dulles since 1962. Neither airport had been treated as a federal priority for capital improvements, and both were falling behind in modernization. Virginia's Republican governor Gerald Baliles and D.C.'s Democratic mayor Marion Barry worked with congressional leadership to create an independent operating entity. The Virginia legislature passed enabling legislation in 1985. The D.C. Council passed its Regional Airports Authority Act the same year. Congress consented in the Metropolitan Washington Airports Act of 1986 - Title VI of Public Law 99-500. Ronald Reagan signed it. The actual transfer of control to MWAA happened on June 7, 1987. Washington National Airport would, in 1998, be renamed Ronald Reagan Washington National Airport in honor of the president who had signed its independence into being.

MWAA's structure was deliberately built to operate without federal appropriations. Daily airport operations, central administration, the police and fire departments, and the payroll are funded through aircraft landing fees, concessions, parking revenue, and rents charged for terminal space. Capital improvements are financed through passenger facility charges collected on airline tickets, federal Airport Improvement Program grants, and bonds the authority issues against future operating revenue. The authority's headquarters sits in Crystal City, less than a mile from Reagan National - close enough that staff can walk to the terminal during a working day. A third major airport serves the region, Baltimore/Washington International Thurgood Marshall, but it remained outside MWAA's jurisdiction. BWI is owned by the state of Maryland, which purchased it from the city of Baltimore in 1972, and is operated through the Maryland Aviation Administration.

In 2008, the authority's responsibilities expanded dramatically. The Commonwealth of Virginia handed over operation of the Dulles Toll Road - State Route 267 - and tasked MWAA with managing the long-stalled project to extend the Washington Metro from East Falls Church to Dulles Airport and beyond into Loudoun County. The route would total 23 miles. Phase 1, opened in 2014, extended the Metro to Reston. Phase 2 brought the line through the Dulles Access Road corridor, up to the airport itself on an elevated viaduct, and out to Ashburn Station in Loudoun County. The project was completed in November 2022. Funding came from a combination of toll revenue on the Dulles Toll Road, federal grants and loans, and contributions from Virginia, Fairfax County, and Loudoun County. The Silver Line is now MWAA infrastructure: built by the authority, owned in part by the authority, operated by WMATA. It connects downtown Washington to Dulles in about an hour.

The lease MWAA holds includes the right-of-way of the Dulles Airport Access Road - the highway built in the early 1960s to connect the new airport to Washington. It was always meant to serve airport traffic only. The inner lanes of State Route 267 remain free and exclusively for travelers heading directly to or from Dulles. The outer lanes were built later by the Virginia Department of Transportation as the Dulles Toll Road, the through-traveler route between the Capital Beltway and Loudoun County. Since 2008, MWAA has owned and operated both - the inner free lanes used only by airport passengers, and the outer toll lanes that fund the Silver Line construction. Drivers in the inner lanes pay nothing. Drivers in the outer lanes pay tolls that, in part, subsidize a Metro line they may never ride.

MWAA runs its own state-accredited police department, with jurisdiction over both airports, the Dulles Access Road, the Toll Road, and a 300-yard buffer around each airport. The Virginia State Police, Fairfax County Police, Loudoun County Sheriff, and Arlington County Police all hold concurrent jurisdiction within their respective borders. The authority also operates its own Fire and Rescue Department, which provides aircraft rescue firefighting, structural firefighting, emergency medical services, and river rescue at National Airport. The department has mutual aid agreements with surrounding Northern Virginia jurisdictions. On September 11, 2001, when American Airlines Flight 77 crashed into the Pentagon - departing from Dulles, striking ground less than two miles from Reagan National - MWAA firefighters from National were among the first emergency responders on the scene. The authority's department, designed for aircraft incidents at its own airports, found itself responding to an aircraft incident at a building that was not one of them. They did. President John E. Potter has run the authority since July 2011 - the latest in a line that began with James Wilding in 1987. The fifty-year lease MWAA signed at its creation will run through June 2037. Renewal will be a question for the next generation.